Prevent_Escape_Chapter_1

seeks to reduce the number of fish that escape from European aquaculture through research to improve fish farming techniques and technologies.

1. ESCAPES

OF

FISHES

FROM

PREVENT ESCAPE is financially supported by the Commission of the European Communities, under the 7th Research Framework Program.

EUROPEAN

SEA- CAGE

AQUACULTURE: ENVIRONMENTAL CONSEQUENCES AND THE NEED TO BETTER PREVENT ESCAPES Cite this article as: Dempster T, Jensen Ø, Fredheim A, Uglem I, Thorstad E, Somarakis S, Sanchez-Jerez P (2013) Escapes of fishes from European sea-cage aquaculture: environmental consequences and the need to better prevent escapes. In: PREVENT ESCAPE Project Compendium.

Chapter 1. Commission of the European Communities, 7th Research Framework Program. www.preventescape.eu ISBN: 978-82-14-05565-8

authors: Tim Dempster1, Østen Jensen1, Arne Fredheim1, Ingebrigt Uglem2, Eva Thorstad2, Stelios Somarakis3, Pablo Sanchez Jerez4 SINTEF Fisheries and Aquaculture, Norway Norwegian Institute of Nature Research, Norway 3 Hellenic Centre of Marine Research, Greece 4 Department of Marine Science and Applied Biology, University of Alicante, Spain 1 2

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THE

RISE OF MODERN AQUACULTURE

In 1971, famous marine explorer and ecologist Jacques Cousteau proclaimed that “We must plant the sea and herd its animals using the sea as farmers instead of hunters. That is what civilization is all about - farming replacing hunting”. Cousteau’s prediction has been borne out dramatically.

Aquaculture is approaching wild fisheries as the major source of fish protein for humans (FAO 2011) through rapid domestication of marine species (Duarte et al. 2008). European aquaculture production has mirrored the global trend, rising from 1 million tons yr-1 in 1990 to >2 million tons y-1 in 2008, principally though producing fish in coastal waters in large net pens (hereafter sea-cages; Figure 1.1). This enormous expansion of aquaculture has multiplied its interactions with the environment in ways Cousteau could never have predicted. Chief among these are the interactions that occur when farmed fish escape from fish farms and enter wild populations.

Figure 1.1. Sea-cage fish farms: above the surface (left) and below (right). Sea-cages can be either square or rectangular and enclose volumes of water typically ranging from 10000-40000 m3.

They may be moored individually or grouped together in multiple systems. Individual cages for many of the main fish species grown now contain anywhere between 10000-400000 fish.

SEA-CAGE AQUACULTURE

AND ESCAPED FARMED FISH

Escapes of fish from sea-cage aquaculture have typically been thought of as referring to juvenile and adult fish. Such escapes have been reported for almost all species presently cultured around the world, including Atlantic salmon, Atlantic cod, rainbow trout, Arctic charr, halibut, seabream, seabass, meagre and kingfish (e.g. Soto et al. 2001, Naylor et al. 2005, Gillanders & Joyce 2005, Moe et al. 2007, Toledo Guedes et al. 2009; Figure 1.2). Recently,

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a second form of escape has come into focus, involving the escape of viable, fertilized eggs spawned by farmed individuals from sea-cage facilities, or so called ‘escape through spawning’ (Jørstad et al. 2008). This phenomenon has forced a redefinition of the term ‘escapes from aquaculture’ to include the escapement of fertilized eggs into the wider marine environment.

Figure 1.2. Escaped seabream (Sparus aurata) beneath a sea-cage (left) and an escape attempt by a cod (Gadus morhua) through a test net mesh panel in Norway (right).

Escapees can have detrimental genetic and ecological effects on populations of wild conspecifics, and the present level of escapees is regarded as a problem for the future sustainability of sea-cage aquaculture (Naylor et al. 2005). For example, over 350 million Atlantic salmon are held in sea-cages in Norway at any given time (Jensen et al. 2010), which outnumbers the approximately 500 000 to 1 million salmon that return to Norwegian rivers from the ocean each year to spawn. In 2010, 291 000 farmed salmon were reported to escape from Norwegian farms, whereas the pre-fishery abundance of wild spawners was estimated at 480 000 salmon (Anon. 2011). A single fish farm cage may hold hundreds of thousands of cultured fish with over a million fish per site within multiple cages now common. Due to the large numerical imbalances of caged compared to wild populations, escapement raises important concerns about ecological and genetic impacts. Evidence of environmental effects on wild populations is largely limited to Atlantic salmon, as these interactions have been intensively studied, with more limited information for the other species farmed across Europe.

ENVIRONMENTAL

CONSEQUENCES OF ESCAPED

ATLANTIC

SALMON

In a comprehensive review of the effects of escaped Atlantic salmon on wild populations, Thorstad et al. (2008) concluded that while outcomes of escapee-wild fish interactions vary with environmental and genetic factors, they are frequently negative for wild salmon. As fish farm areas are typically located close to wild fish habitats, and escaped fish may disperse

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over large geographic areas (e.g. Furevik et al. 1990, Whoriskey et al. 2006, Hansen 2006, Hansen & Youngson 2010), escaped salmon may mix with their wild con specifics and enter rivers tens to hundreds of kilometres from the escape site during the spawning period. The average proportion of escaped salmon in Norwegian rivers monitored close to the spawning period varied between 11 and 35% during 1989-2010 (13% in 2010), with the highest proportions during the late 1980s and early 1990s (Anon. 2011). Consequently, the potential exists for escapees to interact negatively with wild populations, through competition, transfer of diseases and pathogens, and interbreeding. Hindar & Diserud (2007) recommended that intrusion rates of escaped farmed salmon in rivers during spawning should not exceed 5% to avoid substantial and definite genetic changes of wild populations.

TRANSFER

OF DISEASES AND PATHOGENS

Escape incidents may heighten the potential for the transfer of diseases and parasites, which are considered to be amplified in aquaculture settings (e.g. Heuch & Mo 2001, Bjørn & Finstad 2002, Skilbrei & Wennevik 2006, Krkoťek et al. 2007). Escapees from salmon aquaculture in Norway have been identified as reservoirs of sea lice Lepeophtheirus salmonis in coastal waters (Heuch & Mo 2001). Newly-migrated post-smolts are particularly vulnerable for sea lice infestations, and salmon lice may represent a significant threat for some wild Atlantic salmon populations (Revie et al. 2009, Finstad et al. 2011, Gargan et al. 2012). In addition, 60 000 salmon infected with infectious salmon anaemia (ISA) and 115 000 salmon infected with pancreas disease (PD) escaped from farms in southern Norway in 2007, yet whether these precipitated infections in wild populations is unknown. The ability for escaped fish to transfer disease to wild fish depends on the extent of mixing between the two groups, which in turns varies with the life stage, timing and location of the escape (summarized by Thorstad et al.

2008). However, while escaped and wild fish mix, little direct evidence for disease transfer from escapees to wild salmon population has been documented, other than for the possible case of furunculosus, a fungal disease accidently introduced to Norway from Scotland in the 1990s with the transfer of stock and then believed to have been spread from farmed to wild populations by escapees (summarized in Naylor et al. 2005).

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INTERBREEDING Successful spawning of escaped farmed salmon in rivers both within and outside their native range has been widely documented (see review by Weir & Grant 2006). The ability of escaped salmon to interbreed with wild salmon depends on their ability to ascend rivers, access spawning grounds and spawn successfully with wild partners. While the spawning success of farmed female salmon may be just 20-40% that of wild salmon and even lower for males (1-24%; Fleming et al. 1996, 2000), high proportions of escaped fish in many rivers can lead to a high proportion of farm x wild hybrids. Escaped female salmon may also interfere with wild salmon breeding through destroying the spawning redds of wild fish if they spawn later (Lura & SĂŚgrov 1991, 1993).

Wild Atlantic salmon are structured into populations and meta-populations with little gene flow between them, and evidence for local adaptation in wild Atlantic salmon is compelling (reviewed

by Garcia de Leaniz et al. 2007). Farmed salmon differ genetically from wild populations due to founder effects, domestication selection, selection for economic traits and genetic drift (reviewed

by Ferguson et al. 2007). Hybridisation of farmed with wild salmon and later backcrossing of hybrids may change the level of genetic variability and the frequency and type of alleles present. Hence, hybridisation of farmed with wild salmon has the potential to genetically alter native populations, reduce local adaptation and negatively affect population viability and character (Ferguson et al.

2007). Several studies have shown that escaped farmed salmon breeding in the wild have changed the genetic composition of wild populations (e.g. Clifford et al. 1998, Skaala et al. 2006).

Large-scale field experiments undertaken in Norway and Ireland showed highly reduced survival and lifetime success of farm and hybrid salmon compared to wild salmon (McGinnity et al.

1997, 2003, Fleming et al. 2000). The relative estimated lifetime success ranged from lowest for the farm progeny to highest for the local wild progeny with intermediate performance for the hybrids. Farmed salmon progeny and farm x wild hybrids may directly interact and compete with wild juveniles for food, habitat and territories. Farm juveniles and hybrids are generally more aggressive and consume similar resources in freshwater habitats as wild fish (Einum & Fleming 1997). In addition, they grow faster than wild fish, which may give them a competitive advantage during certain life stages. Invasions of escaped farmed salmon have the potential to impact the productivity of wild salmon populations negatively through juvenile resource competition and competitive displacement. Fleming et al. (2000) determined that invasion of a small river in Norway by escapees resulted in an overall reduction in smolt production by 28% due to resource competition and competitive displacement. Local fisheries could therefore suffer reduced catches as wild fish stocks decline (SvĂĽsand et al. 2007).

COMPETITION

FOR FOOD

Escaped salmon consume much the same diet as wild salmon in oceanic waters (Jacobsen & Hansen 2001, Hislop & Webb 1992) and could potentially compete for food with wild stocks. Substantial competitive interactions in the ocean, however, appear unlikely to occur as ocean mortality of salmon appears to be density-independent (Jonsson & Jonsson 2004), although limited information exists to assess if this is also the case for coastal waters (Jonsson & Jonsson 2006).

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ENVIRONMENTAL CONSEQUENCES OF ESCAPED ATLANTIC COD At present, little direct evidence exists for negative interactions of escaped and wild Atlantic cod juveniles or adults, despite predictions that negative consequences will result (Bekkevold et al. 2006). Cod farming is a relatively new industry, thus if negative consequences exist they may not have had sufficient time to manifest and/or be detected. Telemetry studies of simulated cod escapes have indicated that escapees, regardless of whether they originated from stocks of coastal or oceanic origin, mix with wild populations in fjord environments and can move to spawning grounds in the spawning season (Uglem et al. 2008, 2010). Behavioral studies have further indicated that escaped farmed cod are likely to hybridize with wild cod (Meager et al. 2009). However, farmed cod may have limited reproductive success in sperm competition with wild cod, which lowers the risk of genetic introgression from escapees (Skjæraasen et al. 2009).

Other possible ecological effects of escaped farmed cod include increased predation pressure on out-migrating wild salmon smolt (Brooking et al. 2006) and transmission of pathogens and parasites to wild populations (Øines et al. 2006), although direct evidence for these effects is at present lacking. Recaptures of Atlantic cod escapees equipped with acoustic transmitters in local commercial and recreational fisheries in Norway are known to be high (approximately 40%; Uglem et al. 2008), indicating that local fisheries receive temporary increases after escape events and may be partially effective in reducing escaped cod numbers.

POSSIBLE

IMPACTS OF ‘ESCAPE THROUGH SPAWNING’ OF

ATLANTIC

COD

In the culture of Atlantic cod, some fish mature during the first year of culture, while a majority of farmed cod are believed to mature during the second year. This means that almost the entire culture stock in any particular farm has the potential to spawn in sea-cages before they are slaughtered. Spawning of Atlantic cod within a small experimental sea-cage containing 1000 farmed cod and dispersal of their spawned eggs in a fjord system has been demonstrated (Jørstad et al. 2008). In the proximity of this experimental sea-cage, 20-25% of the cod larvae in plankton samples were determined by genetic analyses to have originated from the 1000 farmed cod (Jørstad et al. 2008). Furthermore, preliminary results indicate that 4-6 % of juvenile cod (35-40 cm total length) caught in the area around the farm in following years were offspring of the farmed cod (van der Meeren & Jørstad 2009). This illustrates that if spawning occurs within commercial cod farms where numbers of farmed individuals are far greater, the contribution of ‘escaped’ larvae to cod recruitment within fjord systems may be substantial.

Escape of large quantities of eggs from caged cod could lead to ecological and genetic effects in wild populations (Bekkevold et al. 2006, Jørstad et al. 2008) as; 1) coastal cod populations in some areas of Norway are presently weak, most likely due to overfishing (ICES 2008); 2) coastal cod have a high fidelity to specific spawning grounds (e.g. Wright et al. 2006); and 3) sea-cage cod farms are often located within short distances of known wild cod spawning grounds (Uglem et al. 2008). Recent research also suggests that cod eggs may be entrained in

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the vicinity of the spawning grounds long after spawning (Knutsen et al. 2007). Therefore, there is considerable potential for larvae from escaped cod eggs to experience favourable conditions for survival and recruitment to coastal cod stocks if spawning in sea-cages occurs during the natural spawning season of wild cod.

ENVIRONMENTAL

CONSEQUENCES OF ESCAPED SEABREAM AND SEABASS

For seabream and seabass, knowledge regarding how escapes might affect ecosystems is limited. Intentional releases of cultured seabream for stock enhancement have been reported from the southern Atlantic coast of Spain, and in the Bay of Cadiz (Sanchez-Lamadrid 2002, 2004). Released fish moved less than 10 km from the release point. Good growth rates and condition indices indicate that the released fish adapted to life in the wild and suggest that populations of wild fish could also be altered by released fish. For example, there is correlative evidence of a substantial increase in wild populations of seabream after fish farming began in the Messolonghi lagoon, Greece (Dimitriou et al. 2007). Dempster et al. (2002) found very few seabream near sea-cages in which seabream were being reared, which suggests either low levels of escape or that escapees move rapidly away from the farms to other habitats.

Based on the ecology of seabream and the location of most fish farms in areas close to wild seabream habitats, it is probable that escapees would mix with their wild con specifics.

Consequently, the potential exists for escapees to interact negatively with wild populations, through interbreeding, competition and transfer of diseases and pathogens.

Escaped seabream were frequently recorded/recaptured in the most common natural habitats of this species and stomach analyses indicated that escapees may feed on natural prey from the first day after escape (Arechavala et al. 2012). Seabream are opportunistic feeders, adapting their diets to the food items available (Tancioni et al. 2003). Initially, escaped seabream eat mainly macrophytes and food pellets, but later also feed on common prey such as crustaceans and molluscs. Therefore, escaped seabream have dietary flexibility and feed well in wild environments shortly after they escape (Arechavala et al. 2011).

The only published long-term data available on escapes of seabass indicate that when seabass cultured from western Mediterranean populations escaped in the eastern Mediterranean, they established and maintained distinct populations of the western Mediterranean phenotype

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without introgressing with the local population (Bahri-Sfar et al. 2005). Escapes of seabass in some locations may be particularly problematic, principally where local populations are small or in areas outside the natural distribution of seabass. For example, seabass do not naturally occur in wild habitats around the Canary Islands and their recent appearance there in coastal waters is due to escapes from sea-cages (Toledo Guedes et al. 2009). Escape of seabass from fish farms in such areas is thus an introduction of a non-native species.

The risk of transmission of pathogens through movements of escaped fish in the Mediterranean areas exists, although transmission has not been documented (reviewed by Arechavala et al. 2012a). Infected farmed fish that escape from cages failure might spread pathogens to other cages or farms, and also to both wild fish species that occur naturally in farming areas.

Both seabream and seabass escapees have been observed to swim to adjacent fish farms post release and then disperse to natural habitats (Arechavala et al. 2011, 2012b), suggesting that they are capable of transmitting pathogens to wild populations should they carry them.

The large variety of shared pathogens among wild and farmed fish species and the various pathways of pathogens transmission increase the possibilities of infection.

POSSIBLE

IMPACTS OF ‘ESCAPE THROUGH SPAWNING’ OF SEABREAM

In the Mediterranean region, information about spawning by fish kept in sea-cages is sparse.

In Greece, the largest EU producer of seabream, both the number of fish farms and their production capacity increased over the past decade, accompanied by a substantial decrease in the price of seabream. This industrial development led to structural and functional changes in the rearing process. The time individual fish were farmed increased from just 12 to 18 months before 1995 (Petridis & Rogdakis 1996) to durations of up to 40 months after 1999 (Dimitriou et al. 2007). Gilthead seabream is a protandrous hermaphrodite species and the increased farming duration has resulted in the production of fish of a size compatible with that necessary for fish to reach the stage of sex inversion and female sexual maturation, normally observed at the age of 2-3 years in the wild. The changes in rearing processes have resulted in the presence of large gilthead seabream individuals (larger than 500g) in cages during the normal reproductive period of their wild counterparts (November-March: Bauchot & Hureau 1986). There is evidence that sex inversion and the production of both male and female gametes occur within cages under the present industrial rearing pattern (Dimitriou et al. 2007). A doubling of the population of wild seabream within the Messolonghi lagoon in Greece, based on standardised commercial fishing trap catch returns, correlates with the advent of farming sea-bream to large sizes in the region. Spawning within sea-cages is suspected to have led to greater recruitment to wild seabream stocks (Dimitriou et al. 2007).

Ecological and economic consequences of this population shift have ensued as while more wild sea-bream are now available to the fishery, they are of much smaller mean size resulting in an overall lower economic return to local fishers.

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THE NEED TO BETTER PREVENT THE ESCAPE OF FISH FROM SEA-CAGE FISH FARMS Improved physical containment at marine fish farming sites, through research and development of fish-farming technology, is a central recommendation of many international workshops and forums on the environmental impacts of escapees (Hansen & Windsor 2006). For example, the FP-6 EU Coordinating Action on the ‘Genetic Impact of Aquaculture Activities on Native Populations; GENIMPACT’ has concluded that efforts should be made to prevent escapes, as ‘instead of trying to protect wild populations from escapees, the best logical solution would be to try to prevent escapes. This will rely on technical improvements from the industry …’

(Triantafyllidis et al. 2007). A global report from the Salmon Aquaculture Dialogue on the incidence and impacts of escaped farmed Atlantic salmon in nature (Thorstad et al. 2008) concluded similarly: ‘The most important management issue at present is the need to reduce the numbers of escaped farmed salmon in nature.’ Further, it is a stated goal of both the Norwegian authorities and the Norwegian Fish Farmers Association to reduce escapes of fish to a level where they do not threaten wild populations (Norwegian Fisheries Directorate 2009).

While far less is known about escapes in the Mediterranean Sea and their impacts, the 2007 CIESM Workshop on the impacts of mariculture in the Mediterranean concluded that ‘better information to document the extent of escapes in the Mediterranean is required, while improved methods to trace escapees and prevent escapes need development’ (CIESM 2007).

PREVENTION

AND

MITIGATION

The Prevent Escape project was specifically aimed at assessing the extent and causes of escapes and generating new knowledge through research to help mitigate the effects of escapees on wild populations on a pan-European scale. Solving technical and operational problems related to escapes is dependent on a combination of research into several technological disciplines and biological knowledge related to the behaviour of fish in sea-cages (Figure 1.3).

Figure 1.3. The research approach taken in the Prevent Escape project.

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By conducting research focused on sea-cages and their immediate surroundings, we assessed the detailed technical and operational causes of escape incidents, assessed the extent of escapes of reproductive gametes, juveniles and large fish from sea-cages, determined the inherent biological mechanisms that pre-dispose certain species of fish towards behaviours within sea-cages that make escapes more likely, and documented the dispersal of escapees to better understand how they may be recaptured. Finally, through research on aquaculture structures, materials, designs and operational methods, we have developed new knowledge to prevent escapes and use technologies to recapture fish after they have escaped. Both of these results will assist efforts to mitigate the effects of escapes.

Information from the various components of the project will help benchmark the performance of equipment under farming conditions and thereby improve national and international standards for the design, construction and use of aquaculture equipment. These key pieces of information, when added to existing knowledge, will allow determination of practical, implementable measures to prevent escapes and mitigate the effects of escapees. If prevention and mitigation are more successful, genetic and ecological impacts should diminish.

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CITED

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